Genetic modulation of energy metabolism in birds through mitochondrial function

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1662, 2009, Pages 1685-1693

  Irene Tieleman, B ^a,b   Versteegh, Maaike A ^a   Fries, Anthony ^c   Helm, Barbara ^b   Dingemanse, Niels J ^a   Gibbs, H Lisle ^c   Williams, Joseph B ^c  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Heritability; Intergenomic coadaptation; Metabolic rate; Mitochondrial DNA; Mitochondrial respiration; Selection

Indexed keywords

CELL NUCLEUS DNA; MITOCHONDRIAL DNA;

ADAPTATION; ANCESTRY; BIOENERGETICS; HERITABILITY; METABOLISM; MITOCHONDRION; QUANTITATIVE ANALYSIS;

AFRICA; ANIMAL EXPERIMENT; ARTICLE; ASIA; BASAL METABOLIC RATE; DNA MODIFICATION; ENERGY EXPENDITURE; ENERGY METABOLISM; EUROPE; FEMALE; GENETIC ANALYSIS; GENETIC DIFFERENCE; GENETIC REGULATION; HEREDITY; HERITABILITY; MALE; MITOCHONDRIAL GENOME; MITOCHONDRION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE GENETICS;

ANIMALIA; AVES; SAXICOLA TORQUATA;

ANIMALS; BASAL METABOLISM; BODY SIZE; DNA, MITOCHONDRIAL; FEMALE; GENETIC VARIATION; HYBRIDIZATION, GENETIC; MALE; MITOCHONDRIA; SONGBIRDS;

EID: 66349107987     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.1946     Document Type: Article

References (60)

1. Avise, J. C. & Nelson, W. S. 1989 Molecular genetic relationships of the extinct dusky seaside sparrow. Science 243, 646-648.
2. Bai, Y. D., Shakeley, R. M. & Attardi, G. 2000 Tight control of respiration by NADH dehydrogenase ND5 subunit gene expression in mouse mitochondria. Mol. Cell. Biol. 20, 805-815.
3. Ballard, J. W. O. & Rand, D. M. 2005 The population biology of mitochondrial DNA and its phylogenetic implications. Annu. Rev. Ecol. Evol. Syst. 36, 621-642.
4. Ballard, J. W. O. & Whitlock, M. C. 2004 The incomplete natural history of mitochondria. Mol. Ecol. 13, 729-744.
5. Blier, P. U., Dufresne, F. & Burton, R. S. 2001 Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet. 17, 400-406. (Pubitemid 32545386)
6. Brookes, P. S., Hulbert, A. J. & Brand, M. D. 1997 The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: no effect of fatty acid composition. Biochim. Biophys. Acta Biomembr. 1330, 157-164.
7. Brzek, P., Bielawska, K., Ksiazek, A. & Konarzewski, M. 2007 Anatomic and molecular correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol. Biochem. Zool. 80, 491-499.
8. Crawley, M. J. 1993 GLIM for ecologists. Oxford, UK: Blackwell Scientific Publications.
9. Daan, S., Masman, D. & Groenewold, A. 1990 Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am. J. Physiol. 259, R333-R340.
10. Das, J. 2006 The role of mitochondrial respiration in physiological and evolutionary adaptation. Bioessays 28, 890-901. (Pubitemid 44433752)
11. Davey, G. P. & Clark, J. P. 1996 Threshold effects and control of oxidative phosphorylation in nonsynaptic rat brain mitochondria. J. Neurochem. 66, 1617-1624. (Pubitemid 26090563)
12. Dohm, M. R., Hayes, J. P. & Garland, T. 2001 The quantitative genetics of maximal and basal rates of oxygen consumption in mice. Genetics 159, 267-277. (Pubitemid 32917376)
13. Ellison, C. K. & Burton, R. S. 2006 Disruption of mitochondrial function in interpopulation hybrids of Tigriopus californicus. Evolution 60, 1382-1391. (Pubitemid 44795582)
14. Else, P. L. & Hulbert, A. J. 1985 An allometric comparison of the mitochondria of mammalian and reptilian tissues - the implications for the evolution of endothermy. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 156, 3-11.
15. Elson, J. L., Turnbull, D. M. & Howell, N. 2004 Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. Am. J. Hum. Genet. 74, 229-238.
16. Falconer, D. S. & Mackay, T. F. C. 1996 Introduction to quantitative genetics. New York, NY: Longman.
17. Fontanillas, P., Depraz, A., Giorgi, M. S. & Perrin, N. 2005 Nonshivering thermogenesis capacity associated to mitochondrial DNA haplotypes and gender in the greater white-toothed shrew, Crocidura russula. Mol. Ecol. 14, 661-670. (Pubitemid 40210693)
18. Gessaman, J. A. 1987 Energetics. In Raptor management techniques manual (eds B. A. Pendleton, B. A. Millsop, K. W. Cline & D. M. Bird), pp. 289-320. New Haven, CT: Yale University Press.
19. Gilmour, A. R., Gogel, B. J., Cullis, B. R., Welham, S. J. & Thompson, R. 2006 ASreml user guide. Release 1.0. Hemel Hempstead, UK: VSN International.
20. Helbig, A. J., Berthold, P., MOhr, G. & Querner, U. 1994 Inheritance of a novel migratory direction in central European blackcaps. Naturwissenschaften 81, 184-186. (Pubitemid 24140258)
21. Helm, B., Gwinner, E. & Trost, L. 2005 Flexible seasonal timing and migratory-behavior results from stonechat breeding programs. Ann. NY Acad. Sci. 1046, 216-227.
22. Hill, R. N. 1972 Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J. Appl. Physiol. 33, 263.
23. Houle, D. 1992 Comparing evolvability and variability of quantitative traits. Genetics 130, 195-204.
24. Hulbert, A. J. & Else, P. L. 2005 Membranes and the setting of energy demand. J. Exp. Biol. 208, 1593-1599.
25. Illera, J. C., Richardson, D. S., Helm, B., Atienza, J. C. & Emerson, B. C. 2008 Phylogenetic relationships, biogeography and speciation in the avian genus Saxicola. Mol. Phylogenet. Evol. 48, 1145-1154.
26. Keverne, E. B. 2007 Genomic imprinting and the evolution of sex differences in mammalian reproductive strategies. Adv. Genet. 59, 217-243.
27. King, J. R. 1974 Seasonal allocation of time and energy resources in birds. In Avian energetics (ed. R. A. Paynter), pp. 4-85. Cambridge, MA: Nuttall Ornithological Club.
28. Klaassen, M. 1995 Moult and basal metabolic costs in males of two subspecies of stonechats: the European Saxicola torquata rubicula and the East African S.t. axillaris. Oecologia 104, 424-432. (Pubitemid 3006275)
29. Konarzewski, M. & Diamond, J. 1995 Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution 49, 1239-1248. (Pubitemid 3025694)
30. Korzeniewski, B. & Mazat, J. P. 1996 Theoretical studies on the control of oxidative phosphorylation in muscle mitochondria. Application to mitochondrial deficiencies. Biochem. J. 319, 143-148.
31. Kruuk, L. E. B. 2004 Estimating genetic parameters in natural populations using the 'animal model'. Phil. Trans. R. Soc. Lond. B 359, 873-890.
32. Ksiazek, A., Konarzewski, M. & Lapo, I. B. 2004 Anatomic and energetic correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol. Biochem. Zool. 77, 890-899.
33. Lacy, R. C. & Lynch, C. B. 1979 Quantitative genetic analysis of temperature regulation in Mus musculus. I. Partitioning of variance. Genetics 91, 743-753.
34. Levy, A. 1964 The accuracy of the bubble meter for gas flow measurements. J. Sci. Instrum. 41, 449-453.
35. Lynch, M. & Walsh, J. B. 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates, Inc.
36. Matsuura, E. T., Niki, Y. & Chigusa, S. I. 1993 Temperature-dependent selection in the transmission of mitochondrial-DNA in Drosophila. Jpn. J. Genet. 68, 127-135.
37. McDonald, J. H. & Kreitman, M. 1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652-654. (Pubitemid 21896661)
38. Mishmar, D. et al. 2003 Natural selection shaped regional mtDNA variation in humans. Proc. Natl Acad. Sci. USA 100, 171-176.
39. Nespolo, R. F., Bacigalupe, L. D. & Bozinovic, F. 2003 Heritability of energetics in a wild mammal, the leaf-eared mouse (Phyllotis darwini ). Evolution 57, 1679-1688. (Pubitemid 36953653)
40. Nespolo, R. F., Bustamante, D. M., Bacigalupe, L. D. & Bozinovic, F. 2005 Quantitative genetics of bioenergetics and growth-related traits in the wild mammal, Phyllotis darwini. Evolution 59, 1829-1837. (Pubitemid 41266784)
41. Nichols, D. G. & Ferguson, S. J. 2002 Bioenergetics III. London, UK: Academic Press.
42. Rand, D. M. & Kann, L. M. 1996 Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice and humans. Mol. Biol. Evol. 13, 735-748.
43. Rand, D. M., Haney, R. A. & Fry, A. J. 2004 Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19, 645-653.
44. Rolfe, D. F. S. & Brown, G. C. 1997 Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731-758.
45. Rønning, B., Jensen, H., Moe, B. & Bech, C. 2007 Basal metabolic rate: heritability and genetic correlations with morphological traits in the zebra finch. J. Evol. Biol. 20, 1815-1822.
46. Ruiz-Pesini, E., Mishmar, D., Brandon, M., Procaccio, V. & Wallace, D. C. 2004 Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303, 223-226. (Pubitemid 38057570)
47. Russell, G. A. & Chappell, M. A. 2007 Is BMR repeatable in deer mice? Organ mass correlates and the effects of cold acclimation and natal altitude. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 177, 75-87.
48. Sadowska, E. T., Labocha, M. K., Baliga, K., Stanisz, A., Wroblewska, A. K., Jagusiak, W. & Koteja, P. 2005 Genetic correlations between basal and maximum metabolic rates in a wild rodent: consequences for evolution of endothermy. Evolution 59, 672-681. (Pubitemid 40441332)
49. Schmidt-Nielsen, K. 1997 Animal physiology: adaptation and environment, 5th edn. Cambridge, UK: Cambridge University Press.
50. Song, Z. & Wang, D. 2002 Relationships between metabolic rates and body composition in the Mongolian gerbils (Meriones unguiculatus). Acta Zool. Sin. 48, 445-451.
51. Speakman, J. R. 2005 Body size, energy metabolism and lifespan. J. Exp. Biol. 208, 1717-1730.
52. Tieleman, B. I. 2007 Differences in the physiological responses to temperature among stonechats from three populations reared in a common environment. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 146, 194-199.
53. Tieleman, B. I., Williams, J. B., Buschur, M. E. & Brown, C. R. 2003 Phenotypic variation among and within larks along an aridity gradient: are desert birds more flexible? Ecology 84, 1800-1815.
54. Tieleman, B. I., Dijkstra, T. H., Lasky, J. R., Mauck, R. A., Visser, G. H. & Williams, J. B. 2006 Physiological and behavioural correlates of life-history variation: a comparison between tropical and temperate zone house wrens. Funct. Ecol. 20,491-499.
55. Urquhart, E. 2002 Stonechats. London, UK: Christopher Helm.
56. Veen, T., Svedin, N., Forsman, J. T., Hjernquist, M. B., Qvarnström, A., Thuman Hjernquist, K. A., Träff, J. & Klaassen, M. 2007 Does migration of hybrids contribute to post-zygotic isolation in flycatchers? Proc. R. Soc. B 274, 707-712.
57. Wikelski, M., Spinney, L., Schelsky, W., Scheuerlein, A. & Gwinner, E. 2003 Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc. R. Soc. Lond. B 270, 2383-2388.
58. Wilkins, J. F. & Haig, D. 2003 What good is genomic imprinting: the function of parent-specific gene expression. Nat. Rev. Genet. 4, 359-368.
59. Zink, R. M. 2005 Natural selection on mitochondrial DNA in Parus and its relevance for phylogeographic studies. Proc. R. Soc. B 272, 71-78.
60. Zink, R. M. & Barrowclough, G. F. 2008 Mitochondrial DNA under siege in avian phylogeography. Mol. Ecol. 17, 2107-2121.